CLIMATE RESEARCH
Clim Res
Vol. 34: 93–98, 2007
Published July 19
Vertebrate phenology at similar latitudes:
temperature responses differ between Poland and
the United Kingdom
Tim Sparks1,*, Piotr Tryjanowski2, Arnold Cooke3, Humphrey Crick4,
Stanislaw Ku źniak2
1
Natural Environment Research Council (NERC) Centre for Ecology and Hydrology, Monks Wood, Abbots Ripton,
Huntingdon, Cambridgeshire PE28 2LS, UK
2
Department of Behavioural Ecology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznan, Poland
3
13 Biggin Lane, Ramsey, Huntingdon, Cambridgeshire PE26 1NB, UK
4
British Trust for Ornithology, The Nunnery, Nunnery Lane, Thetford, Norfolk IP24 2PU, UK
ABSTRACT: We examined the phenology of 2 amphibians (common frog Rana temporaria, common
toad Bufo bufo) and one resident bird species (blackbird Turdus merula) at locations in Poland and in
the UK on similar latitudes. The timing of phenology was earlier in the UK than in Poland, presumably as a consequence of a warmer maritime environment. This was further confirmed by the earlier
frog spawn phenology in the warmer west of the UK than in the east. In the amphibians, the response
to temperature was significantly greater in the UK than in Poland, although for the resident bird species the greater response in the UK did not achieve significance. These results suggest that species
are adapted to local conditions. However if such adaptive strategies are not able to evolve rapidly to
match rapidly changing climatic conditions, then severe disruption to the least flexible elements in
any system may result.
KEY WORDS: Rana temporaria · Bufo bufo · Turdus merula · Temperature response rate ·
Climate change · Egg-laying · Spawning
Resale or republication not permitted without written consent of the publisher
In an earlier study, Tryjanowski et al. (2006) reported
on the differential phenological response to temperature between a location in Poland and one in the UK for
2 plant species, the woodland forb Viola reichenbachiana and the ornamental tree Aesculus hippocastanum.
Because the 2 locations were at similar latitudes they
would have very similar light regimes (photoperiod),
so the differences they reported in temperature response seem to be the consequence of local selection
or genetics. It is clear that animals, directly or indirectly,
follow vegetation development and also respond to
temperature (Tryjanowski et al. 2002, Walther et al.
2002, Cummins 2003, Parmesan & Yohe 2003, Rainio et
al. 2006). However, to our knowledge, there has not
been an analysis which focuses on the response of animals to temperature at similar latitudes but under contrasting climate regimes. Because amphibians and
birds are often used in phenological studies (Walther et
al. 2002, Parmesan & Yohe 2003) we decided to use
data on spring activity and/or spawning date of 2
amphibians: the common frog Rana temporaria and
the common toad Bufo bufo, and egg-laying date of
one bird —the blackbird Turdus merula. All 3 are
sedentary species, therefore we predicted that the
effect of local temperature should be stronger than for
long-distance migratory species (Tryjanowski et al.
2002, Parmesan & Yohe 2003, Raino et al. 2006). We
expected that any difference in response between
amphibians and birds should be connected to the different role that temperature plays in determining the
*Email: [email protected]
© Inter-Research 2007 · www.int-res.com
1. INTRODUCTION
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Clim Res 34: 93–98, 2007
phenology of these animals. Because amphibians are
sedentary ectothermic (cold blooded) animals and
because they are sensitive to changes in local ambient
temperature, subtle changes in climate may be reflected in changes in timing and duration of their
hibernation and breeding activity. The blackbird,
whilst sedentary, is more mobile than the 2 amphibians
and may therefore change its wintering place according to the local temperature/food situation.
We extend the earlier study and examine phenological responses in the reproduction of 1 endothermic
(warm blooded) and 2 ectothermic vertebrates. We use
data on first spawning, migration and laying dates,
because these are readily available and have been
found to be robust in previous analyses of phenology
(Sparks et al. 2001).
2. MATERIALS AND METHODS
First observation dates of spawning by common frog
Rana temporaria for 1978–2005 were collected from
3 locations; the environs of the village of Turew in
Poland (centred on ca. 52.1° N, 16.8° E; Tryjanowski et
al. 2003), Huntingdonshire (now part of Cambridgeshire) in eastern England (centred on ca. 52.4° N,
0.1° W) and the village of Kilgetty in Wales (51.7° N,
4.7° W). Records for Turew, sited within an arable landscape, were taken within 5 km of the village. Huntingdonshire is an area of 950 km2 in a largely arable landscape. Records for Kilgetty were taken on a farm in
a pastoral landscape. All sites are at altitudes under
100 m above sea level (a.s.l.). First spawning dates of
common toad Bufo bufo in Turew were obtained for
the same years as for frogs (Tryjanowski et al. 2003).
We could not obtain toad spawning records for a
similar latitude in the UK, so we used dates when peak
numbers of traffic casualties were recorded each
spring, 1978–2005, on roads within 250 m of the breeding pond at Field Road, Ramsey, Cambridgeshire
(52.5° N, 0.1° W; Cooke & Sparks 2004). The peak traffic casualty dates were when peak migration into the
pond had just occurred and are expected to approximate breeding dates. At a nearby colony, where both
migration and spawning were recorded for 11 yr, first
spawning was (on average) a few days earlier than,
and highly correlated (p < 0.001) with, peak migration
date.
Records of first-egg laying dates in blackbird Turdus
merula nests were obtained from Leszno in Poland
(centred on ca. 51.8° N, 16.6° E) and from eastern England (centred on ca. 52.4° N, 0.8° E) from the British
Trust for Ornithology’s Nest Record Scheme (Crick et
al. 2003). For each country the earliest of the first egg
dates (FED) and the number of nest records for each
year from 1978–2004 were extracted. In both cases, the
available datasets are part of a random selection of the
records computerised for national monitoring purposes
and the number of records varied greatly; Poland from
2 to 17 records annually (average 7), England from 1
to 33 records annually (average 17). The number of
records affects the minimum FED in a nonlinear way;
for England the correlation between minimum FED
and sample size was –0.37; that with log sample size
–0.51; thus the analyses below use log sample size to
control for the number of records.
Mean monthly temperatures for the Polish series
were obtained from the Turew meteorological station
(ca. 30 km from Leszno) and for the English series
from the Central England temperature series (www.
metoffice.gov.uk/research/hadleycentre/obsdata/cet.
html). Because the Welsh site is close to the western
coast of the UK, the Central England record may not be
representative here, particularly in winter (Croxton et
al. 2006). Consequently, we obtained temperature data
from Aberporth meteorological station (ca. 45 km distant; 52.1° N, 4.5° W) to compare with data from Kilgetty.
Trends in phenology were assessed by regression on
year to examine for changes over time; those for blackbird FED were assessed after first fitting log sample
size. Temperature responses were examined by regression of phenology on the mean temperature of an
antecedent 3 mo period; for blackbird (after fitting log
sample size) using February–April means; for Polish
and English amphibians using January–March means
and for Welsh frogs using November–January means.
Antecedent periods of 3 mo have previously been
shown to account for most of the phenological temperature response (Menzel et al. 2006). Equality of slopes
was compared using standard regression techniques
(Draper & Smith 1998).
3. RESULTS
All of the 3 mo temperature periods we have used for
the UK experienced a significant increase in temperature, but neither of the 2 Polish periods did so (Table 1).
Table 1. Mean temperatures (± SD), temporal temperature
trends (b; ± SE) and significance of these trends (p) for
November–January (NDJ), January–March (JFM) and
February–April (FMA) 1978–2005 (28 yr)
Period Location
Temperature (°C)
b (°C yr–1)
p
NDJ
Wales
6.4 ± 0.8
0.037 ± 0.017
0.032
JFM
Poland
England
1.0 ± 2.2
5.0 ± 1.4
0.053 ± 0.053
0.092 ± 0.028
0.320
0.003
FMA
Poland
England
4.2 ± 1.6
6.4 ± 1.1
0.037 ± 0.037
0.079 ± 0.022
0.330
0.022
95
Sparks et al.: Vertebrate phenology and temperature
Table 2. Rana temporaria, Bufo bufo and Turdus merula. Frog
and toad spawning and migration dates, and blackbird first
egg date in Poland, England and Wales. L: length of measuring
period (yr); mean dates also given as DOY: day of year (mean
± SD); b: temporal trends (± SE ); p: significance of temporal
trends. Trends for blackbird were examined sequentially
after fitting log sample size
L (yr) Mean date
Frog
spawning
Poland
22
England 28
Wales
23
Toad
spawning
Poland
21
30 Mar
4 Mar
25 Jan
8 Apr
DOY
b (d yr–1)
89 ± 5.3 –0.23 ± 0.13
63 ± 11.6 –0.41 ± 0.27
25 ± 6.7
0.12 ± 0.19
98 ± 4.8
–0.32 ± 0.10
Table 3. Rana temporaria, Bufo bufo and Turdus merula. Response (b; ± SE) and significance of response (p) of frog and
toad spawning and migration dates, and of blackbird first egg
date, to temperatures during 3 mo periods (JFM: January–
March; FMA: February–April; NDJ: November–January).
Responses for blackbird were examined sequentially after
fitting log sample size
p
0.082
0.13
0.54
0.004
Toad
migration
England 28
25 Mar
84 ± 14.6 –0.74 ± 0.32
0.027
Blackbird
first egg
Poland
27
England 27
17 Apr 107 ± 12.7 –0.14 ± 0.24
22 Mar 81 ± 12.6 –0.64 ± 0.28
0.57
0.030
3.1. Frog
None of the trends in the first spawning of frogs was
significant (Table 2, Fig 1), although that from Poland
was marginally significant (p = 0.082). Mean dates
from all 3 sites were significantly different from one
another (assessed by Tukey’s test, following 2-way
ANOVA F2,43 = 430.95, p < 0.001), but there was no significant difference in trends over time (F2,67 = 1.45, p =
0.24). Spawn dates in Wales were particularly early.
There was a significantly greater variability in spawn
dates in England than at the other 2 sites (Variance
Ratio tests, p < 0.005). The 3 sites had significantly different temperature responses (F2,67 = 4.63, p = 0.013)
(Table 3, Fig. 2), UK responses being greater than
Period
b (d °C–1)
p
Frog spawning
Poland
England
Wales
JFM
JFM
NDJ
–1.40 ± 0.37
–4.94 ± 1.31
–3.55 ± 1.72
0.001
0.001
0.052
Toad spawning
Poland
JFM
–0.82 ± 0.43
0.075
Toad migration
England
JFM
–6.95 ± 1.53
< 0.001<
Blackbird first egg
Poland
Wales
FMA
FMA
–2.50 ± 1.04
–3.84 ± 1.83
0.024
0.047
those from Poland. Temperature response in England
may have been accentuated, because the frog increased markedly in abundance during the study
period (Cooke 1999) and so bred at many more sites
during the recent mild springs. The relative high winter temperatures — and hence early spawn dates — in
Wales are evident from Tables 1 & 2 and Fig. 2.
3.2. Toad
Toad peak migration in the UK was significantly earlier than first spawn date in Poland (paired t20 = –5.09,
p < 0.001) (Table 2, Fig. 3) and significantly more variable (Variance Ratio test, p < 0.001). There was a sig-
100
First spawn date (DOY)
90
First spawn date (DOY)
100
90
80
70
60
50
80
70
60
50
40
30
40
20
30
10
–4
20
–2
0
2
4
6
8
Temperature
10
1980
1990
2000
Fig. 1. Rana temporaria. Trends in first spawning dates (day
of year, DOY) of frog in Poland (black), England (grey) and
Wales (dashed)
Fig. 2. Rana temporaria. Relationship between first spawning
dates (day of year, DOY) of the common frog in Poland (black)
and in England (grey) with January–March mean temperature,
and in Wales (dashed, open symbols) with November–January
mean temperature (°C)
96
Clim Res 34: 93–98, 2007
140
110
130
First egg date (DOY)
Date (DOY)
100
90
80
70
60
110
100
90
80
70
60
50
40
50
1980
1990
2000
1
Fig. 3. Bufo bufo. Trends in first spawning dates (day of
year, DOY) of common toad in Poland (black) and peak
migration dates in England (grey)
110
2
3
4
5
6
7
8
Mean February–April temperature (°C)
Fig. 6. Turdus merula. Minimum first egg dates (day of year,
DOY) of blackbird in Poland (black) and England (grey) in
relation to mean February–April temperature (°C)
nificant advance in the dates for both toad records
(Table 2), but no significant difference in the trend
between the 2 sites (F1,45 = 1.30, p = 0.26). Both toad
records showed evidence of a response to temperature,
although the response in Poland was only marginally
significant (p = 0.075) (Table 3). Responses to temperature were significantly different (F1,45 = 16.79, p <
0.001) (Fig. 4).
100
Date (DOY)
120
90
80
70
60
3.3. Blackbird
50
–4
–2
0
2
4
6
8
Mean January–March temperature (°C)
Fig. 4. Bufo bufo. Relationship between first spawning dates
(day of year, DOY) of the common toad in Poland (black) and
peak migration dates in England (grey) with January–March
mean temperature (°C)
140
First egg date (DOY)
130
120
110
Mean minimum FED for blackbird was 26 d earlier in
England than in Poland (paired t26 = –8.03, p < 0.001)
(Table 2). Trends in minimum FED for blackbird are
shown in Fig. 5. After fitting log sample size, a significant trend for earlier laying was detected for England
but not for Poland (Table 2). There was, however, no
significant difference in trends between the 2 countries (F1,49 = 0.46, p = 0.50). Data from both countries
showed a response to mean February–April temperature (Table 3) and while the response from England seemed greater, it was not significantly different
(F1,49 = 0.10, p = 0.75) (Fig. 6).
100
90
4. DISCUSSION AND CONCLUSIONS
80
70
60
50
40
1980
1990
2000
Fig. 5. Turdus merula. Minimum first egg dates (day of year,
DOY) of blackbird in Poland (black) and England (grey) for
1978–2004
The general pattern of earlier phenology and a
response to ambient temperature reported here has
been found widely in both animal and plant studies
(e.g. Walther et al. 2002, Parmesan & Yohe 2003, Menzel et al. 2006), and may be because vertebrate phenology follows trends in vegetation and/or invertebrate
development (Harrington et al. 1999, Walther et al.
2002) in addition to any physiological responses to
Sparks et al.: Vertebrate phenology and temperature
warming (Beebee 1996, Cummins 2003, Crick 2004,
Robinson et al. 2005). This study shows that populations of the same animal species, at similar latitudes
and altitudes, but under different climatic regimes,
can exhibit differences in the scale of phenological
response to temperature. Thus, populations of the
same species appear to be adapted to their climates.
Despite being under the same photoperiodic conditions, populations in the UK, with a maritime climate,
show earlier breeding activity and a greater response
to temperature than populations adapted to a more
continental climate in Poland. There is even evidence
to suggest that this trend occurs between the west and
east of the UK.
It is sometimes difficult to find records of the same
events at similar latitudes, and we are as limited in the
choice of species (and events) here as we were in the
previous study on plants (Tryjanowski et al. 2006). We
were unable to locate records on toad spawning at
similar latitude, but we think that the use of the migration records reported here will not be misleading. Both
spawning and migration responds to temperature
(Beebee 1996). We have used as example species both
ectothermic and endothermic animals, but it would be
unwise to generalise from this small sample.
What is clear is that breeding activity gets underway
earlier in the UK than in Poland for all 3 animals, and
the large differences (ca. 2 mo) in the mean dates of
frog spawning between Wales and Poland suggest that
photoperiod can only play a minor role in this species’
phenology. For the frog and toad it seems that the temperature response in Poland is much more conservative than that in the UK, as we found for 2 plants (Tryjanowski et al. 2006). Because winter temperatures are
lower in Poland relative to the UK (see Table 1) this
suggests that precocious behaviour in Polish animals
would involve high risk, particularly in the amphibians
which only have one breeding attempt per year. Birds
will typically be able to lay repeat clutches if necessary, but at a physiological cost (Whitmore et al. 1977,
Brown & Brown 2000). In the case of amphibians,
experiments to examine breeding behaviour of translocated individuals to confirm these findings would be
an interesting follow-up study.
We suggest that animals in Poland have adapted,
exhibiting conservative behaviour to deal with the
local climate. What is not known is whether these species can modify their phenological response in a period
of a rapidly warming climate, and if so, how quickly.
This fundamental question needs urgent attention as it
could undermine the conclusions of the large number
of climate envelope modelling studies that have been
undertaken around the world (e.g. Harrison et al. 2001)
which assume a fixed relationship between climate and
the distribution of a species.
97
Acknowledgements. We thank 2 anonymous referees for their
comments on an earlier draft of this paper. We are grateful to
M. Rybacki, L. Berger and J. Te˛czyński for help in collecting
field data on amphibians in Poland, to J. Karg for assistance
with obtaining Turew temperature data, and to R. Regelous
for the Kilgetty data. We are very grateful to all the volunteer
birdwatchers who have contributed records to the BTO’s Nest
Record Scheme which is funded under the Joint Nature Conservation Committee (JNCC)/BTO partnership that the JNCC
undertakes on behalf of Natural England, Scottish Natural
Heritage, the Countryside Council for Wales and the Environment and Heritage Service in Northern Ireland.
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Editorial responsibility: Mauricio Lima,
Santiago, Chile
Submitted: March 1, 2007; Accepted: May 25, 2007
Proofs received from author(s): July 10, 2007